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Differentially Expressed Genes Match Bill Morphology and Plumage Despite Largely Undifferentiated Genomes in a Holarctic Songbird

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Differentially Expressed Genes Match Bill Morphology and Plumage Despite Largely Undifferentiated Genomes in a Holarctic Songbird Molecular Ecology (2015) doi: 10.1111/mec.13140 Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird NICHOLAS A. MASON*† and SCOTT A. TAYLOR*† *Department of Ecology and Evolutionary Biology, Cornell University, 215 Tower Rd., Ithaca, NY 14853, USA, †Fuller Evolutionary Biology Program, Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA Abstract Understanding the patterns and processes that contribute to phenotypic diversity and speciation is a central goal of evolutionary biology. Recently, high-throughput sequencing has provided unprecedented phylogenetic resolution in many lineages that have experienced rapid diversification. The Holarctic redpoll finches (Genus: Acanthis) provide an intriguing example of a recent, phenotypically diverse lineage; traditional sequencing and genotyping methods have failed to detect any genetic differences between currently recognized species, despite marked variation in plumage and mor- phology within the genus. We examined variation among 20 712 anonymous single nucleotide polymorphisms (SNPs) distributed throughout the redpoll genome in com- bination with 215 825 SNPs within the redpoll transcriptome, gene expression data and ecological niche modelling to evaluate genetic and ecological differentiation among currently recognized species. Expanding upon previous findings, we present evidence of (i) largely undifferentiated genomes among currently recognized species; (ii) substantial niche overlap across the North American Acanthis range; and (iii) a strong relationship between polygenic patterns of gene expression and continuous phenotypic variation within a sample of redpolls from North America. The patterns we report may be caused by high levels of ongoing gene flow between polymorphic populations, incomplete lineage sorting accompanying very recent or ongoing diver- gence, variation in cis-regulatory elements, or phenotypic plasticity, but do not support a scenario of prolonged isolation and subsequent secondary contact. Together, these findings highlight ongoing theoretical and computational challenges presented by recent, rapid bouts of phenotypic diversification and provide new insight into the evo- lutionary dynamics of an intriguing, understudied non-model system. Keywords: Fringillidae, gene expression, high-throughput sequencing, phenotypic diversity, species limits Received 4 December 2014; accepted 27 February 2015 that different regions of the genome may convey differ- Introduction ent information about the speciation process (Key 1968; Inferring the patterns and processes that accompany the Bazykin 1969; Barton & Hewitt 1981; Rand & Harrison generation of phenotypic diversity and new species is 1989; Harrison & Rand 1989; Harrison 1990; Wu 2001; an overarching goal of evolutionary biology. In recent Nosil & Feder 2012; Seehausen et al. 2014). Moreover, years, evolutionary biologists have embraced the notion the criteria used to delimit species have changed over time—the onset of high-throughput sequencing has pro- Correspondence: Nicholas A. Mason, Fax: (607) 255-8088; vided unprecedented amounts of genetic data that can E-mail: [email protected] be used to infer evolutionary history (Lemmon & © 2015 John Wiley & Sons Ltd 2 N. A. MASON and S. A. TAYLOR Lemmon 2013; McCormack et al. 2013). These novel spread genus of songbirds: the redpoll finches (Acan- technologies provide promising tools to study the evo- this). lution of phenotypic diversity and speciation, particu- The redpoll finch complex currently includes three larly within groups that have experienced recent and species, Acanthis flammea, Acanthis hornemanni and Acan- rapid diversification, which typically lack coalescence this cabaret, which are recognized by most authorities and exhibit incomplete lineage sorting (Maddison & (e.g. Clements et al. 2014; Fig. 1B). However, between Knowles 2006). Such ‘species flocks’ present an ongoing one and six species have been recognized based on challenge for evolutionary biologists to discriminate plumage and morphology (Coues 1862; Harris et al. true speciation events from hybrid swarms and ongoing 1965; Troy 1985; Herremans 1989; Seutin et al. 1992; gene flow, especially when marked phenotypic varia- Marthinsen et al. 2008). Collectively, redpolls are dis- tion is present. tributed throughout the Holarctic and individuals that Reduced-representation approaches, such as double- differ in plumage and morphology (putative species) digest restriction-associated DNA sequencing (ddRAD- frequently co-occur within the Holarctic range of the Seq) and genotyping by sequencing (GBS), are genus. The most widespread taxon, A. flammea, has dar- outperforming traditional Sanger-sequencing methods ker plumage overall, heavily streaked sides and under- in their ability to help us understand the evolution of tail coverts, and a longer, wider bill (Clement 2010a). phenotypic variation in young lineages. Hybridization By comparison, A. hornemanni is lighter with less streak- and incomplete lineage sorting are often common in ing and a stubby, narrower, conical bill (Clement such lineages, which can obscure evolutionary rela- 2010b). The most recently recognized species, A. cabaret, tionships (e.g. Lake Victoria cichlids, Wagner et al. is the smallest of the redpoll taxa and is browner over- 2012; Nicaraguan crater lake cichlids, Elmer et al. all (Knox et al. 2001; Sangster et al. 2002). Acanthis flam- 2014; Heliconius butterflies, Nadeau et al. 2013; Xipho- mea and A. hornemanni are both widespread and phorus fishes, Cui et al. 2013; Jones et al. 2013; wolf- abundant throughout the Holarctic, although A. horne- like canids, vonHoldt et al. 2011; American oaks, Hipp manni is generally found at higher latitudes. Acanthis et al. 2014; Carex, Escudero et al. 2014). Reduced-repre- cabaret was historically restricted to the British Isles, but sentation approaches have also generated evidence of has recently colonized northern mainland Europe and strong genetic differentiation in the absence of obvi- southern Norway. ous differences in plumage and morphology in a Although some studies have suggested geographic widely distributed lowland Neotropical bird species structuring or multimodal distributions of phenotypic (Harvey & Brumfield 2014), provided the resolution variation within the redpolls (Molau 1985; Seutin et al. necessary to robustly test hypotheses about the gener- 1992), other studies have indicated a high prevalence of ation of hybrid species (e.g. Nice et al. 2012) and intermediate phenotypes and overlap in plumage and proved useful for resolving shallow population struc- morphological characters between currently recognized ture in species of conservation concern (e.g. Larson species (Troy 1985; Herremans 1989). Beyond morpho- et al. 2013). logical differences, previous studies have cited differ- In addition to the novel insights gained from ences in vocalizations (Molau 1985; Herremans 1989), restriction enzyme-based approaches, RNA-Seq experi- phenology (Herremans 1989) and physiology (Brooks ments have revealed that gene expression differences 1968) as evidence of multiple species within the com- also play an important role in the speciation process plex. Most recently, Lifjeld & Bjerke (1996) suggested (Wolf et al. 2010). Changes in gene expression often that A. cabaret and A. flammea pair assortatively in underlie phenotypic differences among taxa, and dif- southeast Norway. However, mixed pairs have also ferential gene expression may associate with early been documented (Harris et al. 1965), and the presence stages of the speciation process (Pavey et al. 2010; of hybrid offspring has been debated (Molau 1985). Brawand et al. 2012; Harrison et al. 2012; Filteau et al. Despite phenotypic variation among currently recog- 2013). Interactions among genotypes and the environ- nized species, molecular studies of redpoll populations ment can also affect gene expression, resulting in have consistently failed to document genetic differentia- phenotypic plasticity and polymorphism within a tion (restriction fragment length polymorphisms lineage (West-Eberhard 2005). However, studies that (RFLPs), Marten & Johnson 1986; RFLPs, Seutin et al. evaluate gene expression in addition to variation 1995; mitochondrial control region, Ottvall et al. 2002; among putatively neutral, anonymous loci are scarce. mitochondrial control region and 10 microsatellites Here, we integrate data from reduced-representation Marthinsen et al. 2008). From a biogeographic perspec- libraries with gene expression data to investigate the tive, this lack of genetic variation is unusual; most role of population differentiation and gene expression Holarctic birds demonstrate some degree of phylogeo- in generating phenotypic diversity within a wide- graphic structuring among temperate ecoregions or © 2015 John Wiley & Sons Ltd PHENOTYPIC AND GENETIC VARIATION IN REDPOLLS 3 ABC Common redpoll N ° 80 N ° N70 ° N60 ° Common redpoll 50 Habitat suitability N Low High ° 40 N ° 30 160° W140°W120 °W100 ° W80° W60° W Hoary redpoll N ° 80 N Hoary redpoll ° N70 Species ° Common redpoll Hoary redpoll Count N60 Lesser redpoll 10 ° 50 Habitat suitability Range 20 N Low High ° Breeding 30 40 Resident N Wintering ° 30 160° W140° W120° W100° W80°W60 ° W Lesser redpoll Fig. 1 The redpoll system. (A) Combined Holarctic distribution of redpoll finches. Dark purple indicates breeding grounds, interme- diate purple indicates resident
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